The Diverse Roles of FLOWERING LOCUS C in Annual and Perennial Brassicaceae Species
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REVIEW
published: 15 February 2021
doi: 10.3389/fpls.2021.627258
The Diverse Roles of FLOWERING
LOCUS C in Annual and Perennial
Brassicaceae Species
Wim J. J. Soppe 1 , Natanael Viñegra de la Torre 2,3,4 and Maria C. Albani 2,3,4*
1
Rijk Zwaan, De Lier, Netherlands, 2 Institute for Plant Sciences, University of Cologne, Cologne, Germany, 3 Max Planck
Institute for Plant Breeding Research, Cologne, Germany, 4 Cluster of Excellence on Plant Sciences, “SMART Plants
for Tomorrow’s Needs,” Heinrich Heine University Düsseldorf, Düsseldorf, Germany
Most temperate species require prolonged exposure to winter chilling temperatures
to flower in the spring. In the Brassicaceae, the MADS box transcription factor
FLOWERING LOCUS C (FLC) is a major regulator of flowering in response to
prolonged cold exposure, a process called vernalization. Winter annual Arabidopsis
thaliana accessions initiate flowering in the spring due to the stable silencing of FLC
by vernalization. The role of FLC has also been explored in perennials within the
Edited by:
Brassicaceae family, such as Arabis alpina. The flowering pattern in A. alpina differs
Caroline Dean, from the one in A. thaliana. A. alpina plants initiate flower buds during vernalization but
John Innes Centre, United Kingdom
only flower after subsequent exposure to growth-promoting conditions. Here we discuss
Reviewed by:
the role of FLC in annual and perennial Brassicaceae species. We show that, besides
David Horvath,
Edward T. Schafer Agricultural its conserved role in flowering, FLC has acquired additional functions that contribute
Research Center (USDA-ARS), to vegetative and seed traits. PERPETUAL FLOWERING 1 (PEP1), the A. alpina FLC
United States
Julia Qüesta,
ortholog, contributes to the perennial growth habit. We discuss that PEP1 directly and
Centre for Research in Agricultural indirectly, regulates traits such as the duration of the flowering episode, polycarpic
Genomics (CRAG), Spain
growth habit and shoot architecture. We suggest that these additional roles of PEP1
*Correspondence:
are facilitated by (1) the ability of A. alpina plants to form flower buds during long-
Maria C. Albani
malbani@uni-koeln.de; term cold exposure, (2) age-related differences between meristems, which enable that
albani@mpipz.mpg.de not all meristems initiate flowering during cold exposure, and (3) differences between
meristems in stable silencing of PEP1 after long-term cold, which ensure that PEP1
Specialty section:
This article was submitted to expression levels will remain low after vernalization only in meristems that commit
Plant Development and EvoDevo, to flowering during cold exposure. These features result in spatiotemporal seasonal
a section of the journal
Frontiers in Plant Science changes of PEP1 expression during the A. alpina life cycle that contribute to the
Received: 08 November 2020 perennial growth habit. FLC and PEP1 have also been shown to influence the timing
Accepted: 25 January 2021 of another developmental transition in the plant, seed germination, by influencing seed
Published: 15 February 2021
dormancy and longevity. This suggests that during evolution, FLC and its orthologs
Citation:
adopted both similar and divergent roles to regulate life history traits. Spatiotemporal
Soppe WJJ, Viñegra de la Torre N
and Albani MC (2021) The Diverse changes of FLC transcript accumulation drive developmental decisions and contribute
Roles of FLOWERING LOCUS C to life history evolution.
in Annual and Perennial Brassicaceae
Species. Front. Plant Sci. 12:627258. Keywords: Arabis alpina, FLC, flowering, PEP1, perennial, perpetual flowering, polycarpic growth habit,
doi: 10.3389/fpls.2021.627258 vernalization
Frontiers in Plant Science | www.frontiersin.org 1 February 2021 | Volume 12 | Article 627258
Soppe et al. FLC in Annuals and Perennials
PLANTS HAVE DIFFERENT WAYS OF in expression patterns of environmentally-regulated flowering
USING WINTER COLD TO time genes (Wang et al., 2009; Bergonzi and Albani, 2011;
Koskela et al., 2012; Hyun et al., 2017, 2019; Zhou et al., 2021).
SYNCHRONIZE FLOWERING IN THE Perennials, however, still have to synchronize their annual cycle
SPRING in order to flower and set fruits during favorable environmental
conditions in spring and summer (Falavigna et al., 2019). The
Winter annuals, biennials and perennial species overwinter as environmental conditions that induce flowering in temperate
seedlings or plants and flower in the spring when favorable perennials vary greatly between species, although most of them
environmental conditions return. Annual and biennial species concentrate their flowering season in the spring. For example,
follow a monocarpic life strategy and die after setting seeds once, grapevine, sweet cherry and peach trees initiate flower buds
whereas the majority of perennials are polycarpic and are able during the summer (Figure 1B; Engin and Ünal, 2007; Carmona
to reproduce several times during their life time (Albani and et al., 2008; Vimont et al., 2019). Therefore, spring flowering
Coupland, 2010; Bratzel and Turck, 2015). Low temperatures in these perennials occurs when the flower buds, which were
during the winter are important to enable synchronous flowering initiated the previous year, grow out. Interestingly, the observed
in the spring but generally regulate different stages of the variation in spring flowering between cultivars is not associated
flowering process in monocarpic compared to polycarpic species. with differences in flower bud initiation but rather with the
Winter annuals and biennials require prolonged exposure requirement of prolonged cold exposure that is needed for plants
to cold to accelerate or to enable flowering, a process called to exit the endodormant state that they enter in autumn (Vimont
vernalization. Prolonged cold exposure is effective when it is et al., 2019). In general, bud dormancy can be divided into
applied to imbibed seeds or young seedlings (of winter annual three phases: paradormancy, endodormancy and ecodormancy.
species), or to older plants (of winter annual and biennial species) Paradormancy (also referred as latency) is the stage during
(Lang, 1952; Chouard, 1960). The requirement of cold exposure which the growth of a bud is inhibited by surrounding
for flowering is common in plants adapted to temperate climates organs (Lang et al., 1987). The other stages of dormancy are
and ensures that they will not flower before the winter (Chouard, environmentally regulated, with endodormancy being induced
1960). Vernalization is considered as a preparatory process that and ecodormancy being maintained by environmental cues
has to take place before a plant can initiate flowering in response (Lang et al., 1987). Buds enter endodormancy during the
to increased daylength in the spring (Chouard, 1960). The autumn and throughout this phase their growth is inhibited
effectiveness of vernalization is usually estimated by the reduction by internal signals (Lang et al., 1987). Prolonged exposure to
of days that plants take to flower after returning to growth- low temperatures in the winter is required for endodormancy
promoting conditions (Chouard, 1960). Thus, vernalization release, and once the chilling requirement is met the buds
aligns with the life cycle of winter annual and biennial species transition into ecodormancy (reviewed in Falavigna et al., 2019).
that initiate flowering in the spring (Figure 1A; Chouard, 1960). Bud growth during ecodormancy is inhibited by unfavorable
In A. thaliana, vernalization has also a quantitative effect on environmental conditions and can be reactivated again when
flowering and the duration of cold that is required for the plants experience growth-promoting conditions (Lang et al.,
acceleration of flowering can vary between accessions (Shindo 1987). Overall, prolonged cold exposure is important for bud
et al., 2006; Li et al., 2014). Plants can be vernalized at different dormancy release and synchronized resumption of growth the
temperatures ranging from 0 to 16◦ C (Wollenberg and Amasino, following spring (referred to as budbreak). Exposure to chilling
2012; Duncan et al., 2015). In some habitats, this temperature temperatures for dormancy breaking is considered to be a distinct
range can be achieved during summer or autumn, suggesting that process from vernalization (Chouard, 1960). Specifically, because
plants can be vernalized before the winter (Billings and Mooney, low temperatures during dormancy breaking do not induce a
1968; Duncan et al., 2015; O’Neill et al., 2019). In addition, older phase change that leads to the formation of new kinds of organs
plants show a stronger response to vernalization than young but cause the regrowth of already existing organs (Chouard,
seedlings, suggesting that the developmental stage/age of the 1960). However, there are obvious similarities between both
plant influences its ability to respond to prolonged cold treatment processes, which both require long-term cold to synchronize
(Chouard, 1960). The effect of cold exposure is also reversible spring flowering (Or, 2009; Atkinson et al., 2013) and share a
and plants can devernalize when cold exposure is followed considerable overlap in their molecular pathways (reviewed in
by high temperatures (Chouard, 1960; Périlleux et al., 2013). Horvath, 2009).
This suggests that the flower-promoting role of vernalization There is also a third variant by which low temperatures
can be lost when plants are exposed to exceptionally high lead to flowering. This variant has been observed in several
spring temperatures. Brassicaceae species, including winter oil seed rape, A. alpina,
Polycarpic perennials do not commit all meristems to Arabidopsis lyrata, pak choi, and Brussels sprouts (Chouard,
flowering and are able to maintain growth from one year 1960; Wang et al., 2009; Kemi et al., 2019; O’Neill et al., 2019).
to the next by keeping some meristems in a vegetative state In these species, flower buds initiate and develop during cold
(Albani and Coupland, 2010). Maintenance of vegetative growth exposure, suggesting that vernalization is not only a preparatory
after flowering is determined by the coordinated action of age- process for flowering but also directly regulates the initiation and
related factors, which determine whether individual meristems formation of floral buds (Figure 1C; Chouard, 1960; Wang et al.,
are sensitive to flower-inductive stimuli, and seasonal changes 2009; Kemi et al., 2019; O’Neill et al., 2019). In the perennial
Frontiers in Plant Science | www.frontiersin.org 2 February 2021 | Volume 12 | Article 627258
Soppe et al. FLC in Annuals and Perennials FIGURE 1 | Annuals and perennials initiate floral buds at different times during the year and use winter to synchronize flowering. Cartoons depict the yearly life cycle of (A) a winter annual (e.g., A. thaliana), (B) a woody perennial (e.g., cherry tree) and (C) an herbaceous alpine perennial (e.g., A. alpina). Winter annual A. thaliana accessions induce flowering in the spring. After floral induction (FI), flowering is initiated and floral buds develop (FD) and emerge (FE). In A. thaliana, all steps from floral induction to emergence are very rapid (FI, FD and FE). In perennials, the stages of floral induction (FI) and floral emergence (FE) are temporarily separated. Many woody perennials induce and initiate flowering during summer (FI and FD) but flower buds emerge (FE) in the spring of the next year. In A. alpina, flowering is induced and initiated (FI and FD) during cold exposure in the late autumn, but flowers emerge (FE) after plants return to warm temperatures. In panel (C), green arrows represent vegetative branches and yellow arrows represent flowering branches. Image created with BioRender.com. A. alpina, flowering is initiated during vernalization under short short growing seasons (Diggle, 1997; Meloche and Diggle, 2001). photoperiods (Figures 1C, 2; Wang et al., 2009; Lazaro et al., This modification of the role of vernalization on flowering does 2018). Similarly, field studies in winter oil seed rape demonstrated not seem to be related to the plant life strategy as both annual and that inflorescences are initiated during the autumn in response perennial species have been reported to form flower buds during to low temperatures (O’Neill et al., 2019). In both species, the cold treatment (Chouard, 1960; Wang et al., 2009; Kemi et al., length of the cold exposure is also important for the outgrowth of 2019; O’Neill et al., 2019). flower buds after the return to warm temperatures (Lazaro et al., 2018; O’Neill et al., 2019). Flower buds may still enter dormancy during the winter or grow more slowly due to low temperatures. THE ROLE AND REGULATION OF In field studies using oil seed rape plants, dissection of shoot FLOWERING LOCUS C (FLC) IN apical meristems showed that inflorescence meristems gradually A. thaliana grow during the winter and thus may not be dormant (O’Neill et al., 2019). Although flower buds in such species develop during Several studies in A. thaliana demonstrated that the major autumn, daylength is still important for flowering. As shown regulator of flowering through the vernalization pathway is in A. lyrata, long photoperiods are important for inflorescence the MADS box transcription factor FLOWERING LOCUS C bolting in the spring (Kemi et al., 2019). Ecological studies (FLC) (Michaels and Amasino, 1999; Sheldon et al., 2000). In in alpine species suggest that flower bud development during temperate grasses, which also require prolonged cold exposure cold exposure can be an advantageous adaptive trait in harsh to flower, and also in biennials such as sugar beet, the regulation environments characterized by prolonged snow coverage and of vernalization is mediated by pathways independent of FLC Frontiers in Plant Science | www.frontiersin.org 3 February 2021 | Volume 12 | Article 627258
Soppe et al. FLC in Annuals and Perennials FIGURE 2 | Flower buds in A. alpina are initiated during vernalization. Progression of the shoot apical meristem of A. alpina accession Pajares imaged by scanning electron microscopy (SEM) in (A) plants were grown for 8 weeks in a long day greenhouse, and subsequently transferred to vernalization for (B) 4 weeks (4wVern), (C) 6 weeks (6wVern) or (D) 8 weeks (8wVern). The main shoot apex is vegetative in plants grown in greenhouse conditions or vernalized only for 4 weeks (4wVern) (A,B, highlighted in green). The main shoot apex initiates flowering after 6 weeks in vernalization (C, highlighted in yellow) and inflorescences develop during vernalization (D, highlighted in yellow). In the axils of leaf primordia close to the shoot apical meristem, new vegetative buds are also formed (C,D, highlighted in green). Scale bars correspond to 20 µm (A) or to 200 µm (B–D). Colored boxes represent different growth conditions: the yellow box a long day greenhouse; and the blue box the vernalization at 4◦ C and short days (8 h light: 16 h dark). SEM pictures were modified from the Ph.D. dissertation of Zhou (2019). Image was composed using BioRender.com. (reviewed in Bouché et al., 2017). FLC is a floral repressor lysine 27 residues resulting in a gradual cell-autonomous FLC that is highly expressed in A. thaliana accessions that require silencing (Angel et al., 2011). The B3-binding transcription vernalization to accelerate flowering (Shindo et al., 2006; Li et al., factor VP1/ABI3-LIKE 1 (VAL1) is required for the PHD-PRC2 2014). Prolonged exposure to low temperatures regulates FLC action at FLC (Qüesta et al., 2016; Yuan et al., 2016). After in two ways: (1) by quantitatively repressing FLC transcript cold exposure, the H3K27me3 mark spreads over the entire accumulation and (2) by ensuring that FLC will remain stably FLC locus and ensures maintenance of long-term silencing silenced after plants have returned to warm conditions. The of FLC (Finnegan and Dennis, 2007; De Lucia et al., 2008). major mechanism that drives FLC transcriptional regulation by This spreading of H3K27me3 is enabled by the PHD-PRC2 long-term cold consists of chromatin modifications (reviewed complex and requires the action of the Polycomb protein LIKE in Berry and Dean, 2015). In A. thaliana accessions, non- HETEROCHROMATIN PROTEIN1 (LHP1) that specifically coding cis polymorphisms at the FLC locus underlie variation binds to H3K27me3 marks (reviewed in Costa and Dean, 2019). in the length of cold required to achieve stable silencing of Similar to other MADS-domain proteins, FLC regulates its FLC (Coustham et al., 2012; Qüesta et al., 2020). FLC is downstream genes by binding to conserved CArG-box motifs transcriptionally repressed by long non-coding RNAs (lncRNAs), in their promoters or introns (Deng et al., 2011; Mateos et al., expressed at the locus in response to cold, which play an early 2017). FLC target genes act in different pathways throughout role in the epigenetic silencing of FLC (Heo and Sung, 2011; development, of which several are implicated in flowering (Deng Csorba et al., 2014). A parallel pathway that interprets long-term et al., 2011; Mateos et al., 2017). These include the floral promoter exposure to low temperatures involves the plant homeodomain FLOWERING LOCUS T (FT), that regulates flowering through (PHD) protein, VERNALIZATION INSENSITIVE 3 (VIN3) the photoperiod pathway; SUPPRESSOR OF OVEREXPRESSION (Sung and Amasino, 2004; Wood et al., 2006; De Lucia et al., 2008; OF CONSTANS 1 (SOC1), that regulates several genes involved Swiezewski et al., 2009). VIN3 expression increases gradually in floral transition at the shoot apex; the SQUAMOSA BINDING during cold by a mechanism that is mediated by the NAC PROTEIN LIKE (SPL) family member SPL15, that contributes to transcription factor NTM1-LIKE 8 (NTL8) (Sung and Amasino, reproductive competence and floral transition; and SEPALLATA3 2004; Bond et al., 2009; Zhao et al., 2020). NTL8 protein (SEP3), that regulates flower development (reviewed in Madrid accumulates during cold exposure, due to growth retardation et al., 2020). Stable FLC silencing after vernalization is, therefore, and reduced number of cell divisions that occur at low a key feature to explain the flowering pattern of winter annual temperatures, and upregulates VIN3 transcription (Zhao et al., A. thaliana accessions. This is because the reduced mRNA 2020). Subsequently, VIN3 forms a complex with its homologous levels of FLC allow the activation of floral promoting pathways PHD protein VERNALIZATION5 (VIN5) and the Polycomb that ensure the initiation of flowering in the spring. For Repressive Complex 2 (PRC2) proteins VERNALIZATION2 the life cycle of an annual plant it is important that FLC (VRN2), MSI1, FIE/EED, and the E(z) homologs SWINGER expression is restored in the next generation. In A. thaliana (SWN) and CURLY LEAF (CLF) (reviewed in Berry and Dean, this occurs during embryo development and by the end of 2015). This PHD-PRC2 complex is recruited to the FLC locus embryogenesis all H3K27me3 marks have been removed from the at 3 nucleosomes, covering exon 1 and part of the first intron FLC locus so that the gene is fully reactivated (Tao et al., 2019; (which is called the nucleation region), and methylates H3 Luo et al., 2020). Frontiers in Plant Science | www.frontiersin.org 4 February 2021 | Volume 12 | Article 627258
Soppe et al. FLC in Annuals and Perennials
Arabidopsis thaliana plants that carry weak FLC alleles can requirement to flower (Wang et al., 2009). An interesting
initiate flowering in the autumn due to low starting FLC mRNA feature in perennial Brassicaceae is that FLC is not stably
levels (Hepworth et al., 2020). These genotypes bolt precociously silenced after vernalization, resembling FLC expression patterns
and show higher mortality in the field, which emphasizes the of A. thaliana accessions that require extended vernalization to
importance of FLC in ensuring spring flowering in A. thaliana flower (Wang et al., 2009; Kemi et al., 2013; Baduel et al., 2016;
(Hepworth et al., 2020). In oil seed rape plants, which initiate Qüesta et al., 2020). Unstable silencing of FLC orthologs by
flowering during cold exposure, the starting levels of BnaFLC vernalization has been observed in plants grown in controlled
also negatively correlate with the timing of flower bud initiation environmental conditions (Wang et al., 2009; Kemi et al., 2013;
in the autumn (O’Neill et al., 2019). Cultivars with lower Lazaro et al., 2018) and also in plants experiencing winter chilling
BnaFLC mRNA levels initiate flowering earlier compared to temperatures in the field (Aikawa et al., 2010; Nishio et al.,
cultivars with higher starting BnaFLC mRNA levels (O’Neill et al., 2020). For instance, transcript accumulation of the A. halleri
2019). Interestingly, although oil seed rape plants do not bolt FLC (AhgFLC) is reduced during winter and is upregulated again
precociously, there is a penalty on plant yield if flowering is the following spring (Aikawa et al., 2010). Interestingly, the
initiated earlier in the autumn (Brown et al., 2019). accumulation of the H3K27me3 mark mirrors the expression
patterns of AhgFLC (Nishio et al., 2020). In A. alpina plants
vernalized for 12 weeks, PEP1 (AaFLC) is also temporarily
THE ROLE OF FLC IN THE REGULATION silenced during cold exposure but it is transcriptionally activated
OF FLOWERING IN PERENNIAL again after plants return to growth-promoting conditions (Wang
BRASSICACEAE SPECIES et al., 2009). On the contrary, FLC of the annual close relative
Arabis montbretiana (AmFLC) is stably silenced by vernalization
The role of FLC has been explored in perennial Brassicaceae (Kiefer et al., 2017). Plants carrying introgressions of genomic
species such as A. alpina (Wang et al., 2009; Albani et al., segments containing the AmFLC into A. alpina, indicated
2012), A. lyrata (Kemi et al., 2013), Arabidopsis halleri (Aikawa that, in the same genetic background, PEP1 and AmFLC are
et al., 2010), Arabidopsis arenosa (Baduel et al., 2016), and differentially silenced after vernalization (Kiefer et al., 2017; Hyun
Boechera stricta (Lee et al., 2018). At regions, syntenic to the et al., 2019). The major difference between the A. alpina and
FLC locus in A. thaliana, some of these species contain tandem A. montbretiana FLC orthologs lies in polymorphisms within
FLC copies derived from duplication events after their divergence non-coding regions suggesting that, similar to A. thaliana FLC,
from A. thaliana (Nah and Chen, 2010; Albani et al., 2012). non-coding polymorphisms may confer differences between
A. lyrata has two tandemly duplicated FLC genes (FLC1 and PEP1 and AmFLC in stable silencing by vernalization (Coustham
FLC2), whereas A. arenosa contains one partial and two complete et al., 2012; Kiefer et al., 2017). Within the Arabideae, the annual
FLC copies (Nah and Chen, 2010). In A. alpina a region life strategy arose several times during evolution (Kiefer et al.,
of ∼2 kb at the FLC ortholog, PERPETUAL FLOWERING 1 2017). Phylogenetic studies in different taxa suggest that annuals
(PEP1), has been tandemly duplicated (Albani et al., 2012). This were derived from perennial ancestors, although in some genera
tandem duplication includes the first exon of PEP1 (AaFLC) annuals seem to have switched back to the perennial growth habit
and parts of its promoter and first intron (Albani et al., 2012). (Friedman and Rubin, 2015). We can, therefore, hypothesize
Interestingly, this tandem duplication leads to the production that Brassicaceae annual species may have gained independently
of two overlapping PEP1 transcripts (PEP1a and PEP1b) that cis polymorphisms at FLC non-coding regions to ensure stable
have different transcriptional start sites, using the two tandemly silencing, which is important for the spring-flowering habit.
duplicated first exons (Albani et al., 2012). This finding could In addition to the seasonal cycling of PEP1 mRNA levels,
suggest that duplication events in FLC orthologs may give the perennial behavior in A. alpina is also characterized by a
rise to diverse functions or specialized forms of the protein. strong regulation of age-related factors that determine whether
Nevertheless, tandem duplications in FLC do not contribute to individual meristems will initiate flowering in response to
the perennial life cycle. For example, several FLC orthologs in vernalization or not (Wang et al., 2009; Bergonzi et al., 2013;
both annual and perennial Arabis species contain duplicated Hyun et al., 2019; Lazaro et al., 2019; Zhou et al., 2021).
regions (Kiefer et al., 2017). In addition, even within A. alpina Interestingly, the degree of PEP1 (AaFLC) stable silencing by
not all accessions contain the partial duplication at PEP1 (AaFLC) vernalization has been demonstrated to vary between meristems,
(Albani et al., 2012). depending on whether they initiated flowering during the cold
The role of FLC in flowering in perennial Brassicaceae is exposure (Lazaro et al., 2018). In juvenile meristems that fail
similar to that reported in A. thaliana and other annual Brassicas. to initiate flowering during cold treatment, PEP1 (AaFLC)
FLC1 mRNA levels in A. lyrata are down regulated in response mRNA levels are reduced during vernalization and upregulated
to vernalization and FLC genes are co-localized with QTLs again after plants return to warm temperatures (Wang et al.,
determining flowering time differences between late and early 2011; Lazaro et al., 2018). In this way, PEP1 (AaFLC) ensures
flowering A. lyrata accessions (Kemi et al., 2013). Similarly, maintenance of vegetative growth after vernalization even when
A. alpina accessions carrying lesions in PEP1 (AaFLC) do not meristems develop further and acquire competence to flower.
require vernalization to flower (Albani et al., 2012). The A. alpina The underlying cause of the difference in PEP1 (AaFLC)
pep1 mutant also flowers without vernalization compared to its regulation by prolonged cold exposure between juvenile and
wild type accession Pajares, that has an obligate vernalization adult meristems is not known. In A. thaliana, DNA replication
Frontiers in Plant Science | www.frontiersin.org 5 February 2021 | Volume 12 | Article 627258Soppe et al. FLC in Annuals and Perennials
has been proposed to be essential for the maintenance of FLC (Maurya and Bhalerao, 2017; Vimont et al., 2019). DAM genes
silencing after vernalization (Finnegan and Dennis, 2007; Qüesta are also regulated by epigenetic mechanisms such as histone
et al., 2020). On the same lines, differences in cell division and modifications (Leida et al., 2012; de la Fuente et al., 2015; Saito
DNA replication between meristems may explain the variation et al., 2015) and DNA methylation (Rothkegel et al., 2017). In
observed in PEP1 (AaFLC) stable silencing by cold. In A. alpina, A. thaliana, SVP is a floral repressor that interacts with other
PEP1 (AaFLC) reactivation after vernalization has been shown transcription factors to regulate floral development and flowering
to be facilitated by PERPETUAL FLOWERING2 [PEP2, the time (De Folter et al., 2005; Gregis et al., 2006; Lee et al., 2007;
A. alpina ortholog of APETALA2 (AP2)], a role not previously Balanzà et al., 2014; Mateos et al., 2015). FLC is an interactor
reported for AP2 in A. thaliana (Bergonzi et al., 2013; Lazaro of SVP in A. thaliana and both proteins act together to regulate
et al., 2019). The mechanism for this role of PEP2 (AaAP2) is not flowering time by repressing FT and SOC1 or GA-related genes
known. AP2 in A. thaliana interacts with chromatin remodeling (Lee et al., 2007; Andrés et al., 2014; Mateos et al., 2015). These
factors such as HISTONE DEACETYLASE 19 (HDA19) (Krogan data suggest that SVP or other MADS box genes might have taken
et al., 2012), but has never been associated with histone the role of FLC in woody perennials to regulate developmental
demethylases which could facilitate the upregulation of PEP1 traits related to prolonged cold exposure.
(AaFLC) mRNA levels after vernalization.
Flowering in adult/competent meristems is initiated at about
6 weeks after the start of vernalization (Figure 2; Wang et al., PLEIOTROPIC ROLES OF FLC IN
2009; Lazaro et al., 2018). For plants to flower, however,
exposure to a minimum of 12 weeks of vernalization is PERENNIAL BRASSICACEAE
required as inflorescence meristems should develop further
In addition to the role of FLC in flowering, studies in A. thaliana
during vernalization (Wang et al., 2009; Lazaro et al., 2018).
and other Brassicaceae species demonstrated that FLC has
The molecular mechanisms enabling floral development during
pleiotropic effects on other developmental traits. Pleiotropic
vernalization involve the floral integrator AaSPL15 and increased
phenotypes may be an indirect effect caused by differences in
sensitivity to the growth regulator gibberellin (GA) (Hyun et al.,
flowering behavior adopted by different species and/or may be
2019; Tilmes et al., 2019). PEP1 expression is still not stably
due to direct roles of FLC on other traits. Examples of direct and
silenced after 12 weeks of vernalization, which leads to floral
indirect pleiotropic effects of FLC are reported below.
reversion phenotypes, such as the presence of bracts or flower to
inflorescence reversion (Wang et al., 2009; Lazaro et al., 2018).
Exposure to a minimum of 18 weeks of cold treatment is required Polycarpic Growth Habit and Shoot
to inhibit floral reversion and to stably silence PEP1 (Lazaro et al., Architecture in the Perennial A. alpina
2018). Floral reversion phenotypes are also observed in A. halleri PERPETUAL FLOWERING 1 (AaFLC) contributes to the
plants, although in this species it has not been reported whether polycarpic growth habit and ensures that A. alpina plants
flower buds are formed the previous year (Aikawa et al., 2010; maintain vegetative growth after flowering (Wang et al., 2009).
Nishio et al., 2020). In pep1 mutants all axillary branches flower, suggesting that
Interestingly, A. alpina genes that act in the age pathway PEP1 (AaFLC) regulates the fate of axillary meristems (Wang
to regulate the age-dependent response to vernalization also et al., 2009; Vayssières et al., 2020). This role of PEP1
influence the duration of vernalization required for flowering. (AaFLC) is facilitated by the ability of A. alpina plants to
For example, PEP2, TARGET OF EAT2 (AaTOE2), TERMINAL initiate flowering during vernalization (Figure 2; Wang et al.,
FLOWER1 (AaTFL1), and AaSPL15 determine the age at which 2009; Lazaro et al., 2018). Flower bud development during
plants become competent to flower in response to cold treatment, vernalization is also coupled with the formation of axillary
but also control the duration of vernalization required for meristems in the leaf axils close to the shoot apical meristem
flowering (Wang et al., 2011; Lazaro et al., 2018; Hyun et al., 2019; (Wang et al., 2009; Ponraj and Theres, 2020; Vayssières et al.,
Zhou et al., 2021). The pep2 and Aatoe2 mutants and transgenic 2020). These newly formed axillary meristems develop into buds
lines with reduced function of AaTFL1 (DsRNAi AaTFL1) flower in a basipetal sequence and do not commit to reproductive
when vernalized at a young age (at 3 weeks old compared to development during cold exposure (green in Figures 2C,D; Wang
5 weeks for wild type plants) and require less than 8 weeks of et al., 2009; Ponraj and Theres, 2020; Vayssières et al., 2020).
vernalization to flower (compared to 12 weeks for wild type A. alpina mutants that carry lesions in floral repressors in the
plants) (Wang et al., 2011; Lazaro et al., 2019; Zhou et al., 2021). age pathway (AaTOE2 and AaAP2/PEP2) but also transgenic
In woody perennials, bud dormancy is regulated by a cluster of lines with altered levels of SPLs (e.g., microRNA cleavage-
tandemly duplicated genes, DORMANCY ASSOCIATED MADS- resistant forms of SPL15, rSPL15) have axillary branches at these
BOX 1-6 (DAM1-6) (reviewed in Falavigna et al., 2019). subapical nodes which develop and become reproductive (Hyun
Similar to FLC, DAM genes encode MADS box transcription et al., 2019; Lazaro et al., 2019; Zhou et al., 2021). A closer
factors, but these are more closely related to A. thaliana look at the A. alpina toe2 mutant demonstrated that these
SHORT VEGETATIVE PHASE (SVP) and AGAMOUS-like 24 subapical buds initiate flowering already during vernalization
(AGL24) (reviewed in Falavigna et al., 2019). The expression (Figure 3B; Zhou et al., 2021). This result suggests that the fate
of DAM genes is upregulated during dormancy induction and of the subapical buds is determined during vernalization by the
downregulated during the transition from endo- to ecodormancy age pathway.
Frontiers in Plant Science | www.frontiersin.org 6 February 2021 | Volume 12 | Article 627258Soppe et al. FLC in Annuals and Perennials
also been reported in other perennials (Costes et al., 2014).
The main stem of A. alpina plants consist of zones of basal
axillary flowering branches (V1), axillary vegetative branches
(V3) and dormant buds (V2) (Figure 3A; Lazaro et al., 2018;
Ponraj and Theres, 2020; Vayssières et al., 2020). PEP1 (AaFLC)
contributes to this complex shoot architecture considering that
the pep1 mutant consists only of V1 axillary branches and lacks
the V2 dormant buds and V3 vegetative branches (Figure 3A;
Wang et al., 2009; Vayssières et al., 2020). In wild type plants,
V1 axillary branches behave similarly to the main shoot apex
and initiate flowering during vernalization, when PEP1 mRNA
levels are reduced (yellow arrows in Figure 3B; Wang et al.,
2009; Vayssières et al., 2020). V3 axillary branches arise after
vernalization from buds formed at the subapical nodes during
cold (green in Figures 2C,D; green circles in Figure 3B; Wang
et al., 2009; Lazaro et al., 2018; Ponraj and Theres, 2020;
Vayssières et al., 2020; Zhou et al., 2021). PEP1 determines the
fate of these buds after vernalization (Wang et al., 2009; Lazaro
et al., 2018). Specifically, PEP1 mRNA levels are upregulated
after vernalization to repress flowering and ensure that these
branches will maintain vegetative development (V3 green arrows
in Figure 3B; Wang et al., 2009; Lazaro et al., 2018). V2 buds
follow a different developmental path, in which their growth
is repressed before and after vernalization by paradormancy
(or latency) and their activity is influenced by their position
FIGURE 3 | Shoot architecture in A. alpina is shaped by vernalization and
on the shoot (gray circles in Figure 3B; Vayssières et al.,
PEP1. (A) Representation of wild type A. alpina (WT) and pep1 mutant plants
after flowering. Wild type plants require exposure to long-term cold to flower,
2020). During cold exposure, V2 buds become ecodormant
whereas pep1 mutants do not and can flower directly in greenhouse (blue circles in Figure 3B; Vayssières et al., 2020). The activity
conditions. Flowering wild type plants have a complex shoot architecture, of V2 buds is not directly regulated by PEP1 (AaFLC) but
which is organized in differentiated zones of basal flowering axillary branches rather by the A. alpina ortholog of BRANCHED 1 (AaBRC1),
(V1) that partially senesce; dormant buds (V2); vegetative axillary branches
whose expression increases during and after vernalization (Purple
(V3); and the inflorescence (I). The pep1 mutant lacks this zonation and has
only V1 axillary branches and the inflorescence. (B) Representation of the triangle in Figure 3B; Vayssières et al., 2020). Flowering time
shoot architecture of a wild type plant during its life cycle before, during and genes such as FT in A. thaliana and SPL15 (OsSPL14) in rice
after vernalization. Blue box represents exposure to prolonged cold, whereas have been reported to influence bud activity (Miura et al., 2010;
the time before and after cold exposure is not colored. During long-term cold, Tsuji et al., 2015). PEP1 (AaFLC) might indirectly inhibit the
PEP1 (AaFLC) transcript levels are reduced and both the main shoot apex and
outgrowth of buds in the nodes within the V2 zone. Specifically,
the apices of V1 axillary branches initiate flowering (yellow arrowheads). In
addition, new buds (V3 buds, green circles) are formed in those leaf primordia PEP1 (AaFLC), by repressing flowering in V3 axillary branches,
close to the main shoot apex. These V3 buds (green circles) do not initiate ensures the continuous formation of young leaves that may act
flowering during cold exposure due to the repressive action of the age as an auxin source to inhibit the outgrowth of V2 buds (Red
pathway. After cold exposure, V3 buds give rise to V3 axillary branches, which arrows in Figure 3B; Vayssières et al., 2020). Many studies in
grow vegetatively because PEP1 (AaFLC) transcript levels are upregulated and
repress flowering. The outgrowth of V2 buds is inhibited by paradormancy (or
A. thaliana support the theory that auxin saturation in the
apical dominance) before vernalization (gray circles), by ecodormancy during transport stream of the main stem can inhibit bud outgrowth
cold exposure (blue circles) and by paradormancy (or latency) after plants by blocking auxin transport from lateral sources (Prusinkiewicz
return to growth-promoting conditions (gray circles). The dormancy status of et al., 2009). Dormant buds are always located at the axils of
V2 buds increases during and after vernalization, and is regulated by a
leaves below the zone of V3 vegetative branches, supporting
mechanism that is independent of PEP1 (AaFLC). Increased dormancy in V2
buds correlates with the upregulation of BRANCHED 1 (AaBRC1), a repressor
the hypothesis that V3 branches may become the new auxin
of bud outgrowth (illustrated with the purple triangle). After vernalization, source that represses the outgrowth of V2 buds (Red arrows
increased dormancy in V2 buds is correlated with increased endogenous IAA in Figure 3B; Vayssières et al., 2020). Nevertheless, mutants in
levels in the stem and auxin transport (red arrows). Image created using which V3 branches flower still have a dormant bud zone (Hyun
BioRender.com.
et al., 2019; Zhou et al., 2021). This phenotype can be explained
by the fact that flowering V3 branches still maintain vegetative
development through secondary or tertiary branching and can
Wild type A. alpina flowering plants exhibit a complex shoot still act as auxin sources (Zhou et al., 2021).
architecture in which axillary meristems behave in different Overall, the complex architecture in A. alpina is a result of the
ways and are organized in different zones (Figure 3A; Lazaro effect of prolonged cold exposure on the regulation of flowering
et al., 2018; Ponraj and Theres, 2020; Vayssières et al., 2020). and on bud dormancy, which differs between meristems. These
Zonation patterns of differential bud activity and fate have roles of cold are partially controlled by PEP1 (AaFLC).
Frontiers in Plant Science | www.frontiersin.org 7 February 2021 | Volume 12 | Article 627258Soppe et al. FLC in Annuals and Perennials
Duration of the Flowering Season in the Pleiotropic Roles of Flc in Seed Traits in
Perennial A. alpina A. thaliana and A. alpina
Many temperate perennials restrict the duration of the flowering Plant fitness can be influenced by seed traits such as seed
season to spring and summer. In A. alpina, pep1 mutants and dormancy and longevity. Seed dormancy is defined as the
accessions that carry inactive PEP1 alleles flower perpetually incapacity of seeds to germinate under favorable conditions
(continuously) (Wang et al., 2009; Albani et al., 2012). In the and enables seeds to prevent germination outside the favorable
field, perpetual flowering genotypes with non-functional PEP1 growth season. Seed longevity determines how long seeds
alleles show extended and asynchronous flowering (Hughes remain viable in the seed bank. Monocarpic plants are usually
et al., 2019). Interestingly, these genotypes also exhibit reduced characterized by seeds with higher seed longevity, as seeds
survival in the field, suggesting that PEP1 contributes to constitute their only option to persist in a certain habitat
plant fitness (Hughes et al., 2019). The role of PEP1 on (Thompson et al., 1998).
the duration of the flowering season is a result of the In A. thaliana, several studies using the (low dormant)
upregulation of PEP1 mRNA levels after vernalization. PEP1 accessions Landsberg erecta (Ler) and Columbia (Col) provided
restricts the duration of flowering season by ensuring that no evidence that FLC enhances germination (Figure 4; Chiang
further meristems will initiate flowering after the return to et al., 2009; Auge et al., 2017; Blair et al., 2017). However,
warm temperatures. this positive effect of FLC on germination has not always been
So far, there are only a few studies exploring the regulation observed. Other studies (also using the Ler and Col accessions)
of flowering duration in other perennials. In the Rosaceace, indicated that FLC plays a negative role in germination by
there is natural variation for this trait. Genotypes that follow enhancing seed dormancy (Figure 4; Chen et al., 2014; Chen
either the seasonal flowering habit (and restrict the duration and Penfield, 2018) or that it does not influence dormancy
of the flowering episode) or the perpetual flowering habit (Liu et al., 2011). These different results suggest a role of
(and flower continuously) can be found (Brown and Wareing, FLC in germination and dormancy in A. thaliana that could
1965; Crespel et al., 2002; Albani et al., 2004). In the wild depend on environmental conditions and genetic backgrounds.
strawberry Fragaria vesca and rose, the perpetual flowering This is also suggested by the observation that the germination
habit arose from loss of function mutations in the floral phenotype of FLC depends on the dormancy level of seeds
repressor TERMINAL FLOWER1 (TFL1) (Iwata et al., 2012; (Blair et al., 2017). In addition, these different observations
Koskela et al., 2012). Interestingly, all perpetual flowering
F. vesca accessions contain the same 2 bp deletion in FvTFL1,
suggesting that in F. vesca (but not in A. alpina and
rose) the perpetual flowering habit arose only once during
evolution (Albani et al., 2012; Iwata et al., 2012; Koskela
et al., 2012). It is also worth noting that the perpetual
flowering habit in most genotypes is linked to a loss of
environmental sensitivity for flowering-promoting conditions.
F. vesca accessions that flower seasonally require exposure
to short photoperiods to induce flowering, whereas perpetual
flowering accessions are day neutral (Koskela et al., 2012).
Similarly, seasonal flowering A. alpina accessions require
vernalization to flower, whereas perpetual flowering accessions
can flower without being exposed to vernalization (Wang et al.,
2009; Albani et al., 2012).
FIGURE 4 | The role of FLC in the life cycle of perennial A. alpina and annual
Leaf Traits in the Annual Cardamine A. thaliana. In A. alpina, PEP1 (AaFLC) regulates flowering in response to
hirsuta vernalization and contributes to the perennial life cycle by acting at different
developmental stages and tissues. Starting from seeds, PEP1 acts as a
FLOWERING LOCUS C has been detected in QTL studies
negative regulator of germination and an enhancer of seed longevity (1). Later
to underlie differences in leaf size and complexity in the on, PEP1 represses flowering and ensures that plants will synchronize
annual Brassicaceae Cardamine hirsuta (Cartolano et al., 2015). anthesis with favorable environmental conditions in the spring (2). PEP1 also
Accessions with reduced expression of the C. hirsuta FLC ensures that V3 axillary branches will remain vegetative after flowering (3). The
ortholog (ChFLC) flower early and have leaves with more leaflets role of PEP1 in flowering and maintenance of vegetative development are
repeated every year (4). In Arabidopsis, FLC acts as a floral repressor in
(Cartolano et al., 2015). Interestingly, cis polymorphisms in the accessions that require vernalization to flower. FLC also influences
nucleation region of ChFLC seem to be responsible for the germination in A. thaliana, either positively or negatively depending on the
differences in leaf complexity and flowering time (Cartolano environmental conditions and genetic background. Lines with (→) indicate
et al., 2015). This effect of ChFLC on leaf shape cannot be positive influence and lines with (⊥) indicate negative influence. As in
Figures 1, 3, green arrows represent vegetative branches, yellow arrows
uncoupled from flowering (Cartolano et al., 2015), suggesting
represent flowering branches and gray circles represent dormant V2 buds.
that the leaf phenotype in C. hirsuta may be associated Image created using BioRender.com.
with flowering time.
Frontiers in Plant Science | www.frontiersin.org 8 February 2021 | Volume 12 | Article 627258Soppe et al. FLC in Annuals and Perennials
could be explained by the function of other genes, such scenarios are less relevant as plants can persist longer in
as FT, that control FLC expression during germination and their ecosystems.
independently affect seed germination (Auge et al., 2019). In A. alpina, PEP1 (AaFLC) also influences seed dormancy
To further enhance the complexity by which these flowering and seed longevity. The pep1 mutant alleles have low dormancy
time genes regulate seed traits, FT has also been shown and reduced longevity, suggesting that PEP1 positively regulates
to either enhance or reduce dormancy in different studies these traits (Figure 4; Hughes et al., 2019). The influence of
(Chiang et al., 2009; Chen et al., 2014; Chen and Penfield, PEP1 on seed dormancy seems more consistent in A. alpina
2018). Although complex, the observed phenotypes indicate a compared to that of FLC in A. thaliana. Although there
role for FLC and other flowering time genes in the control has only been a single study of this trait in A. alpina until
of germination. The exact role and mechanism of FLC in now, it showed a consistent role of PEP1 in greenhouse and
germination control is still unclear, but it seems likely to be garden experiments. The existence of many A. alpina accessions
influenced by environmental factors (in particular temperature) with non-functional PEP1 alleles suggests an advantage of
that vary between experiments. This is consistent with the the combination of perpetual flowering and low dormancy in
observation that FLC is maternally controlled in its influence on certain environments.
dormancy (Chiang et al., 2009; Chen and Penfield, 2018). FLC is Overall, the role of FLC in the two major developmental
therefore likely to have a role in the translation of environmental transitions of plants and its adjustment to temperature give
conditions experienced by the mother plant into the dormancy it an important regulatory role to determine the life cycle of
level of its progeny seeds. Brassicaceae species. Additional functions of FLC as described
Although both flowering and germination should be properly in this review also suggest a link between the regulation of
timed to ensure reproductive success, the suppressive role these developmental transitions and the architecture of the
of FLC on flowering seems to be more consistent among plant. This could have selective advantages in nature but also
experiments and species, compared to its role in seed traits. implies that breeding for altered flowering time in Brassicaceae
An interesting difference between these two developmental species could have unexpected effects on seed traits and/or
transitions is that seed germination can be arrested and plant architecture or other still unknown trade-offs. Therefore,
postponed for a year if conditions are unfavorable, which functional studies of this link can provide new insights in the
is not possible for flowering in monocarpic plants. Seed relation between these traits and support breeding for crop
dormancy induction on the mother plant is also more sensitive adaptation to local and changing climates. Whereas FLC has
to subtle differences in ambient temperature compared to been demonstrated to affect different traits in Brassicaceae,
flowering induction. Small differences in temperature before other genes are expected to fulfill its function in other plant
and during seed development can have a strong impact families. For instance, in cereals the VRN genes have a
on seed dormancy (Springthorpe and Penfield, 2015). If similar role in the regulation of vernalization as FLC in the
FLC has a role in translating these subtle temperature Brassicaceae. It would be of great interest to find out whether
differences to dormancy differences, it could explain the these genes also have similar roles in other traits that are
varying phenotypes between experiments. Another difference regulated by FLC. Conservation of this link would indicate its
is that exposure to long-term low temperatures (below 10◦ C) general importance for survival and adaptation of plants to
downregulates FLC transcript accumulation and leads to their environment.
flowering, whereas exposure of plants to mildly low temperatures
(16 versus 22◦ C) before seeds are fully ripe can enhance FLC
expression (Chen and Penfield, 2018). This suggests a different AUTHOR CONTRIBUTIONS
mechanism by which temperature regulates FLC expression,
which could be related with its more flexible role in germination All authors developed the concept and wrote the manuscript.
compared to flowering. NVdIT prepared the figures.
In annuals, FLC regulates both flowering time and
germination traits and therefore constitutes a connecting factor
between both traits. Different scenarios for this connection
FUNDING
can be hypothesized which could be advantageous in different This work was supported by the Cluster of Excellence
climates. The combination of late flowering and low dormancy on Plant Sciences (CEPLAS) funded by the Deutsche
could cause seeds to germinate in autumn and enable the Forschungsgemeinschaft (DFG, German Research Foundation)
plant to survive in a vegetative state during winter. Late under Germany’s Excellence Strategy – EXC 2048/1 –
flowering and high dormancy would delay germination till Project ID: 390686111.
the next spring and enable plants to grow vegetatively during
the year and flower the following spring. Early flowering
and low dormancy would be advantageous in a climate ACKNOWLEDGMENTS
with humid summers and enable two generations within
one year. Early flowering and high dormancy would enable We thank Margaret Kox for critical reading of the manuscript
flowering and seed set in spring and delay germination and Alice Vayssières for contributing in the design of the
until the next spring. In perennials, all these different A. alpina model.
Frontiers in Plant Science | www.frontiersin.org 9 February 2021 | Volume 12 | Article 627258Soppe et al. FLC in Annuals and Perennials
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